Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

Abstract

The ubiquity of outcrossing in plants and animals is difficult to explain given its costs relative to self‐fertilization. Despite these costs, exposure to changing environmental conditions can temporarily favor outcrossing over selfing. Therefore, recurring episodes of environmental change are predicted to favor the maintenance of outcrossing. Studies of host–parasite coevolution have provided strong support for this hypothesis. However, it is unclear whether multiple exposures to novel parasite genotypes in the absence of coevolution are sufficient to favor outcrossing. Using the nematode Caenorhabditis elegans and the bacterial parasite Serratia marcescens, we studied host responses to parasite turnover. We passaged several replicates of a host population that was well‐adapted to the S. marcescens strain Sm2170 with either Sm2170 or one of three novel S. marcescens strains, each derived from Sm2170, for 18 generations. We found that hosts exposed to novel parasites maintained higher outcrossing rates than hosts exposed to Sm2170. Nonetheless, host outcrossing rates declined over time against all but the most virulent novel parasite strain. Hosts exposed to the most virulent novel strain exhibited increased outcrossing rates for approximately 12 generations, but did not maintain elevated levels of outcrossing throughout the experiment. Thus, parasite turnover can transiently increase host outcrossing. These results suggest that recurring episodes of parasite turnover have the potential to favor the maintenance of host outcrossing. However, such maintenance may require frequent exposure to novel virulent parasites, rapid rates of parasite turnover, and substantial host gene flow.

Variation in self-compatibility among genotypes and across ontogeny in a self-fertilizing vertebrate

“…Mixed mating strategies offer the fitness rewards of both outcrossing with conspecifics and fertilizing one's own eggs. The cost-to-benefit ratio of each strategy is expected to vary across space and time as the external and internal environments also change (Maynard Smith 1971;Lively and Lloyd 1990;Lehtonen et al 2012;Layman et al 2017;Lynch et al 2018).…”

No measurable fitness cost to experimentally evolved host defence in the Caenorhabditis elegans–Serratia marcescens host–parasite system

“…These data suggest that multiple loci are involved in conferring elevated host defence, and at least a portion of those loci harbour segregating variation sufficient, even after strong selection for multiple generations. Indeed, the ancestral populations were capable of responding to selection imposed by novel S. marcescens genotypes (Lynch et al ., ). The host mating system and evolutionary histories of the host populations may contribute to this variation in defence.…”

Bridging the gap between theory and data: the Red Queen Hypothesis for sex

“…Through decades of work, Lively et al have demonstrated that the population satisfies necessary conditions for the host-parasite coevolutionary dynamics and provides support for the hypothesis (e.g., Lively (1987Lively ( , 1989; Lively (1995b, 1998); Jokela et al (2009);Vergara et al (2014b); Gibson et al (2016)). While field studies often provide only indirect evidence for the hypothesis, experimental systems can be used to directly test the hypothesis (Auld et al, 2016;Slowinski et al, 2016;Lynch et al, 2018;Zilio et al, 2018).…”